Proc. 15th INA Conf., Bohol, Philippines
J. Nannoplankton Res. 36 (2), 2016, pp.133–136 © 2016 International Nannoplankton AssociationISSN 1210-8049 Printed by The Sheridan Press, USA133

Xenospheres and anomalous coccospheres from plankton
samples of the Southern Indian Ocean
Shramik M. Patil, Rahul Mohan*, Syed A. Jafar, Sahina Gazi
National Centre for Antarctic and Ocean Research (NCAOR), Headland Sada, Vasco-da-Gama, Goa-403804, India; *rahulmohan@ncaor.gov.in
Manuscript received 26th October, 2015; revised manuscript accepted 23rd July, 2016

Abstract New xenospheres and anomalous coccospheres are reported from the plankton samples collectedduring the austral summer (January–February) of 2010 in the Southern Indian Ocean. A new xenosphere consistingof a Calcidiscus leptoporus coccosphere and a Syracosphaera nodosa exothecal coccolith is documented. Anotherxenosphere consisting of different morphotypes of Emiliania huxleyi is illustrated. Additionally, an anomalous
coccosphere of Calcidiscus leptoporus and a coccosphere with very variable sized Oolithotus fragilis coccoliths arerecorded.

Keywords Xenosphere, coccolithophores, anomalous coccospheres, Southern Indian Ocean

1. Introduction
Coccolithophores predominantly produce coccospheres
consistently formed of one or a few types of coccoliths.
However, occasional records of combination coccospheres (consisting of two or more types of coccoliths
which do not normally co-occur) have been recorded since
the beginning of 19th century (Lohmann, 1902; Kamptner,1940; Lecal-Schlauder, 1961), as reviewed by Cros et al.
(2000a). These have now been shown to record life-cycletransitions (Cros et al. 2000b) and, owing to limited culture studies, the documentation of genuine combination
coccospheres in recent years has added significantly to therecognition of life-cycle associations and led to changes
in nomenclatural taxonomy based on the rules of priority (e.g. Alcober & Jordan, 1997; Cros et al., 2000b; Croset al., 2000a; Cros & Fortuño, 2002). These combination
coccospheres are typically heterococcolith-­holococcolith
combinations (Kleijne, 1991; Thomsen et al., 1991;­Billard, 1994; Cros et al., 2000a; Cortés, 2000; Cortés &Bollmann 2002; Geisen et al., 2002; Frada et al., 2009)and less frequently heterococcolith-nannolith combinations (Cros et al., 2000b; Sprengel & Young, 2000).
During the terminology workshop of the 4th INA
Conference (1991) in Prague, the concept of combination coccospheres was discussed. The term ‘xenosphere’
was proposed by Jackie Burnett and recommended it for
the terminology guide that ultimately followed (Younget al., 1997). The term xenosphere was defined therein as:“Anomalous coccosphere containing coccoliths, normallyregarded as forming on quite discrete species”. This term
was redefined by Young & Geisen (2002): “Specimens
resembling coccospheres but which include coccoliths of
discrete species, which are unlikely to have been produced
as a result of a life-cycle change or hybridization event”.
Coccolithophores thrive in marine waters co-occurring with a ­variety of organic (zooplankton, picoplankton, bacteria and virus) and inorganic particles with low

gravitational sinking rates but active brownian movement, electrical forces and surface tension. In such ascenario, postmortem and fragmental remains of natural
coccospheres float around in close vicinity. Live coccolithophores probably adopt a strategy of certain marine
zooplankton, which use hydromechanical/biochemicalcues to sense prey, predator, mate, light, etc. (Visser, 2001;Harvey et al., 2013). If strange coccoliths are biologically picked up then inserted and arranged in a naturalconfiguration (concave-­down convex-up orientation) thenbiogenic inclusion is a strong possibility (Young & Geisen,
2002: Plate 1, figs. 1–2, Emiliania huxleyi and Gephyrocapsa oceanica). In contrast, if the strange coccolith isinserted side-ways or in a concave-up convex-down orientation then accidental inclusion in high density preparationmaterial is a strong possibility (Young & Geisen, 2002)
and, therefore, such examples are unlikely to be true combination coccospheres and may instead be xenospheres.
2. Material and methods
Xenosphere examples illustrated herein were observed in
the plankton samples collected during the 4th Indian Southern Ocean Expedition (January-February, 2010) within thearea 30°S–65°S (~48°E and 57.3°E transects).
Vertical water samples were collected using Niskinbottles attached to a Conductivity Temperature Depth­(CTD) rig between the surface and 110m water depth. One
litre of water was collected in a clean, prewashed plastic
bottle and immediately vacuum filtered through Whatman
Nuclepore Track-Etched membrane filters (47mm diameter, 0.2µm pore size) using a Pall filtration unit. The filter membranes were further dried in an oven at 45°C for
48 hours and kept in Millipore sterile petri dish until analysis.
In the laboratory at NCAOR (National Centre for
Antarctic and Ocean Research), a small piece of filter
membrane (~5mm2) was cut and placed on a double sided
carbon tape attached to a 1 cm diameter aluminum stub

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and sputter coated with platinum (~2nm thick). The sample was inspected under a JEOL JSM-6360LV ScanningElectron Microscope (SEM) at 2,000x magnification using 5–15KV accelerating voltage.
3. Examples
3.1 Xenosphere: Calcidiscus leptoporus
coccosphere with Syracosphaera nodosa
exothecal coccolithThis specimen shows numerous Calcidiscus leptoporus
heterococcoliths and a single smaller wheel-like coccolith.
The smaller coccolith is about 2µm across and appears tobe planar with a distinct medial cycle of oblique laths. Thisis almost certainly a Syracosphaera nodosa exothecal heterococcolith and, given the simple rim, is identified as Syracosphaera nodosa type A sensu (Young et al., 2003). The
S. nodosa exothecal coccolith (Pl. 1, fig. 1 [a]) is lying innormal orientation on a C. leptoporus coccosphere (Pl. 1,fig. 1 [b]) and is covered by C. leptoporus coccoliths on
one side, with no sign of forcing.
3.2 Xenosphere: Emiliania huxleyi
morphotype combination
This specimen shows the combination of morphologicallydifferent Emiliania huxleyi coccoliths (Pl. 1, fig. 2 [a,b]). Thiscoccosphere consist of numerous coccoliths of E. huxleyi

Plate 1All images were captured with a JEOL JSM- 6360 LV Scanning Electron Microscope at the NCAOR, Goa, India. All plankton samples were collected(0-110m depths) during 4th Indian Southern Ocean Expedition.
Fig. 1. Xenosphere of S. nodosa (a) and C. leptoporus exothecal coccoliths (b); 44°S, 57.3°E; 60m depth.
Fig. 2. Xenosphere of E. huxleyi morphotypes: (a) large (b) normal; 43°S, 57.3°E; 60m depth.
Fig. 3. Calcidiscus leptoporus twin coccosphere; 46°S, 57.3°E; Surface.
Fig. 4. Oolithotus fragilis morphotypes: (a) large (b) small; 43°S, 57.3°E; 60m depth.

Xenospheres and anomalous coccospheres…of the Southern Indian Ocean

morphotype O (Hagino et al., 2011) and a single, heavily
calcified E. huxleyi morphotype A coccolith. Examination of
the coccosphere reveals the presence of various E. huxleyi
morphotype O coccoliths with different sizes (distal shieldlength [L] and width [W] was about 2.7 and 2.3μm, respectively). This size range was comparable to other E. huxleyi‘O’ morphotypes recorded in the same sample (L = 2.6–3.0μm; W = 1.8–2.6μm). The large E. huxleyi morphotype
A (L = 3.58μm, W = 3.19μm) observed is included in thecoccosphere in a perfectly regular fashion and overlappedby normal morphotype O coccoliths. This suggests selectionand inclusion onto coccosphere by biological process.
Combinations of E. huxleyi and G. oceanica wereillustrated in the previous studies by Clocchiatti (1971),
Winter et al. (1979), Young & Geisen (2002: Plate 1,figs 1–2; Plate 2, fig. 3), and also by EMIDAS (http://www.emidas.org).

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represent accidental clustering caused during preparation
techniques; however, clustering of coccoliths/coccospherein faecal pellets are not included in this discussion.
Unlike heterococcolithophore-holococcolithophorecombinations, which basically represent the natural twophase life-cycle, xenospheres are abnormal coccospheres,
largely resulting from the accidental inclusion of strange
coccoliths, but also possibly by rare involvement of biologic process (see Harvey et al., 2013). The anomalous
coccosphere combinations represent unusual coccosphere
formation with variations in coccolith-coccosphere sizeand shape.
The selection and elegant incorporation of G. oceanica
coccoliths into E. huxleyi coccospheres, as documented
in previous studies, does not appear to be accidental but
designed by biological process, thus more rigorous experimental studies of live coccospheres could usefully becarried out in the future.

3.3 Anomalous coccosphere: Calcidiscus
leptoporus double-cell
Acknowledgements
In addition to the above mentioned examples of co-­ The authors are thankful to the Secretary, Ministryoccurrence, we also observed occasional abnormally large of Earth Sciences (MoES), Government of India andCalcidiscus leptoporus coccospheres (Pl. 1, fig. 3 [a]). the ­Director, National Centre for Antarctic and Ocean
Coccospheres of C. leptoporus usually consist of about ­Research for supporting the Past Climate and Oceanic
14–26 placoliths (Young et al., 2003) but the present ex- variability group. We would also like to thank the Chiefample shows the association of more than 42 placoliths. Scientist and the expedition members of the Southern
The formation of twin coccospheres during normal asex- Ocean cruise for the support extended for our sampling
ual binary division of the cell has previously been de- needs. We gratefully acknowledge Captain Satishraja
scribed (e.g. Klaveness, 1972), and likely explains this Rangaraja, Ebin James and other crew members of ORV
type of coccosphere observed here.
Sagar Nidhi, for their support during the expedition. Theauthors would like to thank the editor and both review3.4 Anomalous coccosphere: Oolithotus
ers for their valuable comments. Dr. Shramik would
fragilis coccoliths
like to thank DST Inspire for providing funding. This is
A broken coccosphere of O. fragilis consisting of large, NCAOR Contribution no. 31/2016.
medium and small coccoliths (except one, the proximal
shield was visible on all O. fragilis coccoliths). The diam- Referenceseter of the proximal shield of O. fragilis coccoliths varied Alcober, J. & Jordan, R.W. 1997. An interesting associationfrom 2.8–4.7μm (Pl. 1, fig. 4 [a,b]). The present example
between Neosphaera coccolithomorpha and Ceratolithus
shows that the coccosphere formation is independent ofcristatus (Haptophyta). European Journal of Phycology,
the size of the coccoliths and is not caused by accidental
32(1): 91–93.
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Clocchiatti, M. 1971. Sur I’existence de coccosphères portant des4. Summary
Xenospheres continue to fascinate and challenge us, andexperimental evidence (e.g. Harvey et al., 2013) is needed
to properly understand the mechanisms involved in theirformation. Based on the forms documented here and a survey of the relevant literature, we hypothesize that, akin to
the strategy adopted by marine zooplankton, coccolithophores may adopt hydromechanical/biochemical cues tosense the postmortem remains of coccoliths and incorporate
these into the living coccosphere in the proper orientation.
Besides this biological strategy, other xenospheres may

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